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Carbonate Precipitation under Pressure for Bioengineering in the Anaerobic Subsurface via Denitrification Derek Martin,*,† Kevin Dodds, Ian B. Butler, and Bryne T. Ngwenya School of Geosciences, Grant Institute, University of Edinburgh, The King’s Buildings, Edinburgh EH9 3JW, U.K. S Supporting Information *

ABSTRACT: A number of bioengineering techniques are being developed using microbially catalyzed hydrolysis of urea to precipitate calcium carbonate for soil and sand strengthening in the subsurface. In this study, we evaluate denitrification as an alternative microbial metabolism to induce carbonate precipitation for bioengineering under anaerobic conditions and at high pressure. In anaerobic batch culture, the halophile Halomonas halodenitrificans is shown to be able to precipitate calcium carbonate at high salinity and at a pressure of 8 MPa, with results comparable to those observed when grown at ambient pressure. A larger scale proof-of-concept experiment shows that, as well as sand, coarse gravel can also be cemented with calcium carbonate using this technique. Possible practical applications in the subsurface are discussed, including sealing of improperly abandoned wells and remediation of hydraulic fracturing during shale gas extraction.

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detrimental to the activity of the urease enzyme itself.18 Furthermore, injection of CO2 into the subsurface for CCS will use supercritical CO2 at a pressure ≥7.4 MPa, which imposes a minimum pressure requirement for microbes to be able to survive during MICP. An alternative microbial metabolism to ureolysis is denitrification, whereby nitrate is used by microorganisms to anaerobically oxidize an organic compound for energy and cell growth. Denitrification increases the pH in the surrounding medium by using H+, according to the general equation

INTRODUCTION Microbially induced carbonate precipitation (MICP) in the subsurface is currently an active area of research and potentially has a number of diverse applications, such as remediation of heavy metals in soils,1,2 modification of groundwater flow,3,4 geotechnical engineering,5−7 and carbon sequestration.8,9 Much research has focused on the model ureolytic bacterium Sporosarcina pasteurii, often with the intention of introducing this organism into the subsurface with a supply of calcium and urea in solution. S. pasteurii produces the enzyme urease, which catalyzes the hydrolysis of urea into ammonium and carbonate with a concomitant increase in pH; consequently, CaCO3 is precipitated out of solution and into the surrounding matrix, binding particles together and helping to stabilize porous media.6,10 One of the major advantages of using in situ microbial mineral precipitation is that it is likely to promote a wider spatial distribution of precipitation than precipitation brought about by the direct addition of an alkaline chemical.11 In addition, bacteria and nutrient solutions may be able to penetrate further into a pore system than a higher viscosity cement/grout. Although S. pasteurii has been used as a model organism in numerous laboratory studies, its long-term use under anaerobic conditions has recently been questioned12 and the stimulation of natural ureolytic communities may be preferable.13−15 Although ureolysis and MICP in seawater has been shown in S. pasteurii,16,17 the applicability of using ureolytic organisms for bioengineering at higher salt concentrations, for example, in deep saline aquifers which may be used for carbon capture and storage (CCS), is unknown (notwithstanding the concerns of using S. pasteurii under anoxic conditions). An additional problem exists in that the byproduct of ureolysis is the environmentally toxic ammonium, the buildup of which may be © 2013 American Chemical Society

electron donor + NO3− + H+ → HCO3− + H 2O + N2

which favors carbonate precipitation where a favorable cation has been supplied and the medium becomes saturated with respect to the mineral in question; consequently, the process can be used for bioengineering in the subsurface where no oxygen is present.19 Sources of nitrate and/or cations, such as calcium nitrate, are readily dissolved in water and are therefore amenable for use in MICP. Additionally, complete denitrification leads to the production of inert nitrogen gas as the eventual end waste product. Most ureolytic MICP research proposing its use in the (deep) subsurface is based on ambient or low-pressure data, though some very recent work has shown MICP at more relevant pressures. Mitchell et al.20 have shown CaCO3 formation at 7.5 MPa using S. pasteurii grown in standard growth medium (low salinity), although they did test the stability of the mineral precipitates themselves in super critical Received: Revised: Accepted: Published: 8692

March 22, 2013 June 7, 2013 June 26, 2013 July 9, 2013 dx.doi.org/10.1021/es401270q | Environ. Sci. Technol. 2013, 47, 8692−8699

Environmental Science & Technology

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CO2 saturated brines. Cunningham et al.21 have also reported MICP at 7.5 MPa in a small 25.4 mm diameter sandstone core under axial flow, and a larger sandstone core under radial flow at 4.2 MPa (equivalent to that used by Phillips et al.7 at atmospheric pressure); however, no detailed results are published as yet. Here we investigate the use of microbial denitrification at high salinity and at actual pressures likely to be used in CCS to explore whether MICP would be feasible under these conditions. A sand column experiment was also performed at ambient pressure to determine the suitability of this process for MICP and biocementation of the sand. The species used for this study was Halomonas halodenitrificans, a halophilic facultative anaerobe that has previously been shown to precipitate CaCO3 when grown aerobically at atmospheric pressure.22,23

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triplicate and pressure experiments in duplicate (due to the size constraints of the pressure vessels). Experiments were destructively sampled at each time point. The pH was measured immediately after the reaction vessels were opened. Subsamples were filtered through a 0.45 μm filter into 2% HNO3 for calcium analysis via ICP-AES (Perkin-Elmer, Optima 5300DV). Any minerals attached to the side of the vessels were scraped off and the samples were then centrifuged (22 000g, 10 min), and the pellet resuspended and washed with deionized water; this was repeated twice then the pellet was dried at 50 °C. Carbonate analysis of the samples was performed on preweighed pellets via coulometry (UIC inc, CM 5012 coulometer with a CM 5130 acidification module). Sand Column. The column consisted of a 500 mm length of polycarbonate tube with an internal diameter of 240 mm giving a total volume of 22.6 L. A 3 cm layer of granite gravel/ chippings (irregular shape, ∼10 mm maximum length) was placed in the bottom to allow even distribution of the input medium and prevent blockage of the influent hole. Carbonatefree silica sand was packed into the column under water to exclude air bubbles, and a 3 cm layer of gravel placed on top of the sand before the column was sealed. The pore volume was ca. 8 L, which represented a porosity of 36%. The medium used was based on that used in batch experiments but with less peptone (1.25 g L−1) and yeast extract (2.5 g L−1) to reduce the phosphorus in the medium and enhance carbonate precipitation (see Results and Discussion). The medium was amended with 100 mM CaCl2·2H2O as a source of calcium, and, as with the batch experiments, the calcium and other constituents were prepared separately, autoclaved, and mixed together in carboys when cooled to prevent calcium precipitation during preparation. All media was made anaerobic by continually sparging with sterile nitrogen. An initial 8 L inoculum of H. halodenitrificans, grown in calcium-free medium (∼48 h), was pumped in through the bottom of the column and left for 24 h before proceeding with further inputs. Medium was pumped into the bottom of the column at a rate of ∼10 L day−1 using a peristaltic pump. Samples of effluent were taken at various times for analysis of dissolved calcium via ICP-AES (0.45 μm filtered samples, stored in 2% HNO3), and nitrate in the effluent was periodically measured semiquantitatively using nitrate test strips (Precision Laboratories, USA, detection limit of 0.2 mM). At the end of the experiment, ∼4.5 pore volumes of water were pumped through the column to remove the growth medium. The column was disassembled and the sand sampled at various depths. Each layer of sand removed was thoroughly mixed and carbonate analysis performed on a subsample of the mixed sand via coulometry. Sand samples were mounted on stubs, sputter coated with gold, and examined on a Philips XL30CP SEM to observe the precipitated minerals (Supporting Information).

MATERIALS AND METHODS

The strain used in all experiments was Halomonas halodenitrificans (NCIMB 700). Batch Cultures. A preliminary experiment investigating the growth of H. halodenitrificans at various pressures was performed to assess its suitability for further study. The growth medium consisted of (L−1) 10 g of yeast extract, 5 g of peptone, 1 g of glucose, 75 g of NaCl, 1.01g of KNO3 as a nitrate source, 1.93 g of calcium acetate, and 18.01 g of magnesium acetate. The experiment was performed in glass vials sealed with crimped butyl septa and inoculated with 0.1 mL of an exponentially growing culture. The vials were completely filled (∼58 mL) to remove all gas bubbles so that pressure could be transferred across the septum. Each treatment was performed in triplicate and all incubations were carried out at 30 °C. Pressurization was achieved hydrostatically in stainless steel vessels via a manual piston screw pump using water as a pressurizing fluid. Experiments were destructively sampled after 96 h and the optical density at 600 nm measured using a Camspec, M501 UV/vis spectrophotometer. Subsequent experiments investigating CaCO3 precipitation were based on the ‘MC’ medium used by Sánchez-Román et al.23 The base medium consisted of (L−1) 10 g of yeast extract, 5 g of peptone, 1 g of glucose, 75 g of NaCl, 5.05 g of KNO3, and 6.12 g of sodium acetate, and CaCl2·2H2O was added as required to obtain different concentrations of calcium. Sodium acetate was used to replace the acetate provided by calcium acetate in the original medium (to allow manipulation of the calcium concentration). The calcium chloride solution was prepared separately to the other constituents to prevent precipitation during heat sterilization. Equal volumes of nutrients and CaCl2·2H2O were prepared separately to 2× strength. Both solutions were sterilized by autoclaving (121 °C, 15 min) and then cooled while being sparged with sterile nitrogen gas (0.2 μm filter). After cooling, both solutions were mixed and the final pH set to 7 using 1 M NaOH solution. 100 mL aliquots were dispensed aseptically and under nitrogen to maintain anoxic conditions. For those at ambient pressure, glass vials sealed with crimped butyl septa were used. For pressure experiments, modified 100 mL syringes were used, whereby the back arm of the plunger was shortened (leaving the piston face still in place) to allow them to fit into pressure vessels and the luer end plugged with a silicon stopper. Syringes/vials were inoculated as required with 0.2 mL of an exponentially growing culture and incubated at 30 °C (where required, pressure was applied as above). Ambient experiments were performed in

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RESULTS Batch Experiments. H. halodenitrificans growth does not become greatly inhibited until a pressure of >20 MPa is applied. Growth declines as the pressure is increased, until at 40 MPa the measured absorbance was the same as that at the start of the incubation period, and growth was completely inhibited over a period of 96 h incubation (Figure 1). Experiments were performed using initial concentrations of 5, 10, 15, and 20 mM calcium; however, the actual concentration was not realized in situ (Supporting Information,

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dx.doi.org/10.1021/es401270q | Environ. Sci. Technol. 2013, 47, 8692−8699


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Figure 1. Growth of H. halodenitrificans at various pressures measured as optical density (data points represent the mean of triplicate replicates after 96 h incubation).

Figure 2. Rate of removal of calcium from solution during growth of H. halodenitrificans at ambient pressure (▲) and 8 MPa (□). Each data point represents mean calcium removal at the maximum observed rate and error bars show standard deviation. Regression line for ambient pressure (---) log y = log 2.1885x + log 1.57, R2 = 0.979, and 8 MPa (•••) log y = log 2.2474x + log 1.6201, R2 = 0.983.

Figure S1), presumably due to the precipitation of small quantities of calcium phosphate(s) (phosphate is present in the yeast extract and peptone, see Discussion). After inoculation, there was a lag phase of about 36 h during which time the pH decreased slightly in all of the treatments. Subsequently, the pH increased to over 8 in all treatments in 2−6 h. This pH increase was accompanied by a decrease in dissolved calcium, but no CaCO3 precipitation was observed where the initial calcium content was 5 mM. A small amount of CaCO3 was observed in the 10 mM, 8 MPa treatment, whereas no CaCO3 was observed in the 10 mM ambient pressure treatment; this may be a reflection of the highest pH observed between the two treatments, with a pH of 8.29 at 8 MPa and 8.18 at ambient pressure. CaCO3 precipitation was observed in all of the other treatments where the initial calcium was ≥10 mM (Table 1).

constant. Figure 3 shows that by reducing the phosphorus content to one-quarter original concentration (original

Table 1. Maximum Yield of CaCO3 Precipitateda CaCO3 precipitated (mmol L−1)

a

init calcium concn (mM)

ambient

8 MPa

5 10 15 20

0 0 3.5 ± 1.0 4.9 ± 0.1

0 1.5 ± 0.3 4.5 ± 0.3 4.8 ± 0.6

See Supporting Information, Figure S1.

Figure 2 shows the maximum measured calcium removal rates for each separately measured initial calcium concentration. The two treatments were compared via an analysis of covariance in the software package “R” using treatment as a factor and log rate as the dependent variable. Obviously, the initial calcium concentration has a significant (P < 0.001) effect on its rate of removal from solution, with higher rates observed where the initial calcium concentration is higher. The slopes of the regression lines are not significantly different (p = 0.93) showing that calcium removal rates are similar at both ambient and 8 MPa pressure. The regression equations show that both treatments display a second-order rate of reaction with respect to the initial calcium concentration. Further experiments were conducted reducing the phosphorus concentration in the medium by reducing the amount of yeast extract and peptone, while keeping all other components

Figure 3. Yield of CaCO3 obtained after incubation of H. halodenitrificans for 7 days at different phosphorus concentrations (full P concentration = 4.5 mM, starting Ca concentration for all treatments = 20 mM). Data represents the mean of triplicate replicates and error bars show the standard deviation.

concentration ∼4.5 mM) a greater than 3-fold increase in the amount of CaCO3 precipitated was obtained. Column Experiment. No nitrate was measured in the effluent at any point, demonstrating that the system remained anaerobic and substantial denitrification had taken place. Dissolved calcium in the effluent decreased to ∼70 mM throughout the experiment, meaning that ∼30 mM of calcium was being removed from solution as the medium was pumped through the column (Supporting Information, Figure S2). 8694



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Figure 4. Cementation of the sand column. (A) The entire base of the column adjacent to the inlet was cemented by extensive CaCO3 precipitation. (B) In order to remove the cemented material from the column it had to be broken into three parts. (C) The cemented material comprised granite gravel and quartz sand. (D) Sand throughout the column was cemented to a lesser degree than the base of the column and a semicontinuous core of sand approximately 30 cm in length was recovered from above the strongly biocemented basal zone.

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When the column was broken up for analysis, the bottom ∼10 cm of the column was uniformly cemented across the diameter of the column, including the gravel filter that had been placed on the bottom to enable even distribution of the input medium and to prevent the influent hole from becoming blocked (Figure 4). The rest of the column did contain CaCO3, although no substantial homogeneous cementation of the upper layers was observed, which was reflected in the mass of CaCO3 observed at various depths (Figure 5). However, cementation did occur throughout the column at different depths, but formed as fingered reaction fronts or zones that were laterally and medially discontinuous (Figure 4D).

DISCUSSION

The initial pressure−growth response data (Figure 1) showed that H. halodenitrificans could grow at a pressure of up to about 20 MPa before any significant inhibition was observed. Subsequently, we chose a pressure of 8 MPa for comparison with ambient pressure, since this is the minimum pressure that would be used for the injection and storage of supercritical CO2 into underground formations.24 Carbonate Precipitation Starts Earlier under Anaerobic Conditions. H. halodenitrificans has previously been shown to mediate the precipitation of calcium carbonate within 4 days when grown aerobically at the salt concentration used in this study, using an initial calcium concentration of 23 mM.23,24 Here we show that calcium carbonate is precipitated under anaerobic conditions in about 36 h, even where the initial calcium concentration is lower than that used by SánchezRomán et al.23 and also at a pressure of 8 MPa (Supporting Information, Figure S1). Under aerobic conditions, bacterial degradation of acetate and glucose produces elevated concentrations of CO2 which initially suppresses pH, before degradation of peptone and yeast extract in the medium releases ammonium, causing a pH increase and subsequent precipitation of CaCO3.23 Under anaerobic conditions, the denitrification process itself increases pH, and pH can begin to increase as soon as denitrification begins and enough cell mass has been produced to overcome any small initial pH decrease due to CO2 production. Accordingly, the shorter time to precipitation under anaerobic conditions is likely to be due to a faster pH increase in the medium rather than any inherent fundamental difference between aerobic and anaerobic metabolism per se. The time to initial CaCO3 precipitation is a function of the cell metabolism and would have been quicker if a larger inoculum had been used.

Figure 5. CaCO3 content as a percentage of total mass at various depths in the column (each data point represents the bottom depth of that particular layer). 8695



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entire nitrate pool was consumed; consequently, a significant pH increase may only have occurred in the bottom of the column. Since the sand was not sterile, as the nitrate was used up this would have allowed for the stimulation of other heterotrophs, given that the organic load of the medium was still high; consequently, the growth of fermenting organisms is likely to have suppressed the pH as the growth medium was pumped further through the column. In addition, the precipitation of CaCO3 itself releases H+ ions into the medium, suppressing pH as the denitrification rate slowed further up the column. When the growth medium was flushed out at the end of the experiment, the pH did increase significantly to 8.1, suggesting that the lower part of the column was at a higher pH. Further experiments increasing the calcium and nitrate concentration and/or reducing the organic load, to a point where H. halodenitrificans was able to grow and deplete the organic material in the full depth of the column, could determine the optimum conditions for cementation. Lowering the organic load would help to distribute nitrate further through the column since microbial activity would not be so intense at the influent. The discontinuous cementation above the bottom plug may be an example of reactive infiltration instability29 or reaction front fingering.30 In this case, the reaction front fingering is a result of both physical flow processes and microbial denitrification promoting CaCO3 precipitation. Flow fingering develops because of extensive CaCO3 precipitation and permeability alteration in the cemented plug formed immediately above the fluid inlet. Flow focusing results in preferential flow paths for nutrients within the porous media, promoting fingered flow fronts in which pH is raised sufficiently to precipitate CaCO3. Extensive gas production observed in the column (N2 and CO2) would also exacerbate the formation of preferential flow paths, though, to a certain extent, this effect will be diminished in the field since more gas will dissolve into the surrounding fluid at the increased pressure in the subsurface. The development of biocementation and flow focusing proximal to injection points for nutrients may present practical problems by restricting permeability pathways in the deep subsurface. However, this has been an active area of research in subsurface bioremediation for a number of years; for example, modeling,31 laboratory,32,33 and field studies34 have shown that, when treating nitrate-contaminated subsurface water using denitrification techniques, temporal separation of nutrient inputs reduces biomass clogging at injection points and provides a more homogeneous distribution of inputs. This same principle has now been applied by Ebigo et al.,28 Phillips et al.,7 and Tobler et al.35 to homogeneously distribute CaCO3 in porous media using S. pasteurii. Practical Implications. CO2 has been shown to be trapped in natural formations for millions of years36,37 and CO2 injection into depleted hydrocarbon reservoirs is likely to pose little risk of leakage, since, by their very nature, they have previously stored hydrocarbons for millions of years, although the act of recovering hydrocarbons does cause fracturing and the wetting properties of CO2 are different from gas and oil. However, the volume of CO2 storage required and the economics of a supply infrastructure will require CO2 injection into new sites, such as deep saline aquifers, where storage integrity may not be comparable. One of the potential risks to CCS is the possibility of CO2 leakage caused by, e.g., undetected faults or fractures in the capping rock, the presence of historic unmapped wells providing a conduit for flow, or

The rate of calcium removal from solution was similar whether H. halodenitrificans was grown at ambient pressure or 8 MPa (Figure 2). Calcium started to precipitate out of solution once enough biomass had grown and pH had increased accordingly; consequently, once calcium removal had been initiated, it took only ∼6 h for the calcium concentration to decrease to the point where no more calcium was precipitated out of solution under the prevailing conditions in the medium (Supporting Information, Figure S1). Calcium removal is a second-order reaction with respect to initial calcium concentration (Figure 2) and the bulk precipitation from solution is pH dependent. Although H. halodenitrificans was isolated from bacon curing brine at ambient pressure, the results demonstrate that H. halodenitrificans is piezotolerant and could be used to precipitate CaCO3 at pressure in the anaerobic subsurface, assuming a source of calcium is available. Although precipitation has been shown at 8 MPa in this study, H. halodenitrificans is tolerant to much higher pressures (see Figure 1), suggesting that CaCO3 precipitation would be possible at higher pressures (preliminary qualitative tests (not shown) demonstrate the precipitation of CaCO3 at a pressure of 15 MPa). Phosphate Compromises MICP. At low concentrations of calcium, no carbonate was precipitated from solution (Table 1, and Supporting Information, Figure S1) since the saturation index of the medium at the pH observed in the experiments was too low for CaCO3 precipitation. However, calcium was removed from solution in all treatments, but even where CaCO3 was precipitated, the reduction in dissolved calcium was not necessarily stoichiometrically proportional to the amount of CaCO3 precipitated from solution. Calcium ion activity may have been reducedand, therefore CaCO3 precipitation reducedby Ca2+ complexation with dissolved organic carbon released from metabolites and/or extracellular polymeric substances produced by the bacteria.25,26 Calcium phosphate(s) were also likely to precipitate due to the high phosphorus content in the medium, which leads to oversaturation of PO43− ions. Sánchez-Román et al.23 calculated that the saturation index for hydroxyapatite was 12 times higher than CaCO3 in equivalent aerobic media (open to the atmosphere). Reducing the phosphorus concentration led to a 3-fold increase in the yield of CaCO3 (Figure 3) and it was for this reason that reduced phosphorus medium was used in the sand column experiment to maximize CaCO3 precipitation. Further experiments would be required to ascertain how far phosphorus could be reduced before affecting bacterial growth rates and/or CaCO3 precipitationa balance would have to be struck to obtain the most efficient MICP relevant to the prevailing field conditions and nutrients already in situ. Precipitation Dynamics under Flow Conditions. The large column test was performed as a proof of concept of the system. H. halodenitrificans was able to cement the bottom part of the column adjacent to the influent, including coarse gravel; however, cementation was spatially variable and not as pronounced above this (Figures 4 and 5). This same spatial variation has been observed in sand columns using ureolysis as a means of MICP.27,28 The pH observed in the effluent may have been lower than that in situ in the bottom of the column (the effluent pH fluctuated between 6.7 and 7.1 throughout the experiment). Nitrate was not detected in the effluent, demonstrating that nitrate was limiting in the column. Denitrification may only have been taking place in the bottom of the column before the 8696



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even thermal fracturing of seals caused by CO2 cooling.38 In addition, CCS may be perceived by the public to be dangerous due to the possibility of leaks, especially if CO2 is injected near or beneath inhabited areas, although the actual risks may be very small.39 Thus, it is imperative to develop remediation measures that will allow leaks to be plugged before attempts at subsurface injection proceed.40 Moreover, even if CO2 is not directly leaking to the surface, subsurface leaks into different strata, such as potable aquifers, may pose problems due to changes in pH and subsequent mobilization of toxic metals or changes to the subsurface ecosystem, or injection of CO2 may displace brines into overlying potable aquifers. Phillips et al. 7 have shown the potential for using biocementation to seal rock fractures by using S. pasteurii as a model organism to seal a hydraulically fractured sandstone core. They showed that MICP was able to seal a fracture that could withstand a pressure 3 times greater than the pressure that originally produced the fracture. While the use of S. pasteurii in small areas where oxygenated media can be provided may be a valid treatment method, the use of S. pasteurii for larger, more diffuse, treatment areas in the anaerobic subsurface may be questionable,12 and, in practice, stimulation of in situ ureolytic organisms may be preferable.13,14 This study shows that H. halodenitrificans could be used for bioengineering in the subsurface and may prove to be a better prospect than using ureolysis for, e.g., CO2 leakage reduction7,9 since it is able to grow at high salt concentrations, under anaerobic conditions, and at elevated pressure. Growth of H. halodenitrificans has been shown at NaCl concentrations between 3 and 20% and at a pH as low as 5,41 so the acidified conditions generated at CCS sites by dissolved CO2 should not prove to be detrimental. Denitrification may have a number of applications for subsurface remediation/bioengineering. Microbial plugging can be used to improve the sweep efficiency during enhanced oil recovery (EOR).42,43 Nutrients injected into a reservoir will preferentially reach high permeability regions, and, consequently, microbes will be stimulated in these areas, impeding preferential flow paths. A number of studies have shown that nutrient additions to injected water, with or without coinjection of bacteria, can seal off high permeability zones and extend the life of an oil field by redirecting displacement fluid into previously bypassed portions of the reservoir.44−47 To rapidly boost biomass production, inoculation with an external strain of denitrifier may be preferential where the hydraulic retention time is short, or where the relevant indigenous organisms are not present.48 Denitrification could also be used to precipitate CaCO3, which is more stable than bacterial cell mass and extracellular polysaccharides, which are susceptible to degradation or damage by high velocity fluid flows.49 This may help to reduce costs in the long term since a continuous input of nutrients would not be required. Cementation can also be useful to prevent well collapse or excessive sand extraction in areas where the natural rock is poorly cemented.50 Additionally, calcium may not have to be added to the process water depending on the concentration already in the formation water. Injection of nitrate to modify permeability has the added bonus that it has been shown to suppress the activity of sulfatereducing bacteria (SRB), since nitrate-reducing bacteria competitively inhibit SRB,51−54 thus preventing oil souring and negating the requirement to use biocides in the EOR process water. Microbially induced cementation may be particularly advantageous for sealing diffuse areas with loosely defined

fracture regions where cement/grout is impeded due to the flow conditions in the subsurface. For instance, records of old abandoned wells are sometimes nonexistent or lost55 and many historic oil and gas wells were never plugged, so they leak gas, oil, and/or brine into freshwater aquifers and the surface environment.56 Bioengineering may be particularly useful in these areas since microbes and ingredients for MICP could be administered to high permeability regions for in situ carbonate precipitationthe exact leakage pathway may not need to be determined beforehand. This technique may also be applicable to shale gas production. Shale gas has become increasingly important in recent years, the production of which requires extensive hydraulic fracturing of the subsurface. MICP may prove to be a particularly useful remediation tool to help constrain the fracture area and prevent gas and process water migration into potable water supplies.57,58 Phillips et al.7 have already demonstrated in “mesoscale” laboratory experiments the sealing of a hydraulic fracture in sandstone using aerobic, ureolytic MICP. Denitrification may be particularly advantageous in the field given that, unlike ureolysis where toxic ammonium is produced, the waste product is inert nitrogen gas, which will have little environmental impact. The method could be used to direct fluid flow elsewhere and reduce the risk of process and saline fluid ingress into potable aquifers (careful control of inputs should allow denitrification to run to completion and prevent excessive production of nitrite). Bioengineering needs to be tailored to the particular circumstances to determine the concentration of nutrients required, the injection regime, the type of organism to be used, or whether natural communities can be stimulated in situ. Ultimately, treatment type will be dependent on the suitability and economic feasibility for a given set of circumstances. Major costs will be an organic feedstock, a source of nitrate, and possibly a calcium source (depending on the ionic composition of the formation water); so, for example, feedstock could be supplemented with waste products. For instance, ∼260 mg L−1 nitrate may be available from typical wastewater sewage after the nitrification treatment step,59 which would result in ∼10% cost saving relative to the nitrate concentration used in this study. H. halodenitrificans adds to the possible suite of options available for MICP. We present evidence that it can mediate the precipitation of CaCO3 under highly saline conditions, anaerobically and at pressures of up to 8 MPa. We also show that MICP via denitrification can cement coarse gravel, as well as fine sand, which has the potential to be used for stabilization and to reduce permeability and seal fractures in the subsurface. Further research will be required to optimize the process and assess its suitability under different circumstances.

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ASSOCIATED CONTENT

S Supporting Information *

(1) Time course of carbonate precipitation. (2) Dissolved calcium analysis of the effluent from the sand column. (3) Scanning electron micrographs of solidified sand and gravel. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Tel.: +44 (0)131 6508608. E-mail: [email protected]. 8697



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School of Physics & Astronomy, University of Edinburgh, James Clerk Maxwell Building, The King’s Buildings, Edinburgh EH9 3JZ, UK. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Funding was provided by the European Union’s Seventh Framework Programme (FP7/2007-2013) under Grant Agreement 226306.

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